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O'Shea, O.R., Thums, M., van Keulen, M. and Meekan, M. (2012) Bioturbation by stingrays at Ningaloo Reef, Western Australia.

Marine and Freshwater Research, 63 (3). pp. 189-197.

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Bioturbation by stingrays at Ningaloo Reef, Western Australia

Owen R. O'Shea A B D, Michele Thums A C, Mike van Keulen B and Mark Meekan A

A Australian Institute of Marine Science, UWA Oceans Institute (MO96), 35 Stirling

Highway, Crawley, WA 6009, Australia.

B Murdoch University, 90 South Street, Murdoch, WA 6150, Australia.

C School of Environmental Systems and Engineering, UWA Oceans Institute,

University of Western Australia M470, 35 Stirling Highway, Crawley, WA 6009,

Australia.

D Corresponding author. Email: o.oshea@aims.gov.au

Abstract

Stingrays are an important part of the biomass of the fishes in shallow coastal

ecosystems, particularly in inter-reefal areas. In these habitats, they are considered

keystone species – modifying physical and biological habitats through their foraging

and predation. Here, we quantify the effects of bioturbation by rays on sand flats of

Ningaloo Reef lagoon in Western Australia. We measured the daily length, breadth

and depth of 108 feeding pits over three 7-day periods, created by stingrays

(Pastinachus atrus, Himantura spp. Taeniura lymma and Urogymnus asperrimus) in

Mangrove Bay. Additionally, an area of ~1 km2 of the lagoon at Coral Bay was

mapped three times over 18 months, to record patterns of ray and pit presence. Over

21 days at Mangrove Bay, a total of 1.08 m3 of sediment was excavated by rays,

equating to a sediment wet weight of 760.8 kg, and 2.42% of the total area sampled,

or 0.03% of the whole intertidal zone. We estimate that up to 42% of the soft

sediments in our study area would be reworked by stingrays each year. Based on a

model predicting the probability of pit presence over time, there was a 40%

probability of ray pits persisting for 4 days before being filled in but only a 15%

probability of a pit being present after 7 days. Changes in pit volume over time were

static, providing evidence for secondary use. Our results imply that rays play an

important ecological role creating sheltered habitats for other taxa in addition to the

turnover of sediments.

Additional keywords: coral reef, Dasyatidae, feeding, pit, ray, soft-sediment,

volume

Introduction

In the vast soft-sediment environments of the oceans, great numbers of species are

bioturbators, creating, shaping and modifying the physical and biological properties

of this habitat. Typically, this is done through behaviours such as feeding, digging or

burrow formation by animals such as crabs (Eggleston et al. 1992), worms

(Mermillod-Blondin & Lemoine 2010), sea cucumbers (Shiell & Knott 2010),

urchins (Needham et al. 2010), dugongs (Nakaoka et al. 2002), turtles (Lazar et al.

2010), teleosts (Hall et al. 1990), elasmobranchs (Valentine et al. 1994) and even

whales (Oliver & Slattery 1985).

Of the elasmobranchs, rays are one of the most obvious and ubiquitous fishes that act

as bioturbators. This diverse group of cartilaginous fishes (over 600 living species)

occupies marine ecosystems from the Arctic to the tropics (McEachran & Dunn

1998; McEachran & Fechhelm 1998; Frisk 2010). In shallow coastal and nearshore

environments the Dasyatidae, or stingrays, are abundant and inhabit soft-sediment

habitats ranging from mangroves to sandy shores and coral reefs (Snelson Jr et al.

1988; Gilliam & Sullivan 1993; Cartamil et al. 2003). The dorso-ventral

compression of rays is thought to assist these animals to exploit shallow tidal areas

for prey (Matern et al. 2000) where they feed by jetting water and beating pectoral

fins to access infaunal and meiofaunal communities in soft sediment, a process of

bioturbation that typically produces conspicuous feeding pits.

Rays frequently occur in large schools when feeding and migrating (Peterson et al.

2001), consequently they have the potential to exert a significant impact on both the

physical environment and biological communities that inhabit soft-sediment habitats.

Feeding activity by rays on intertidal and subtidal sediments can significantly reduce

benthic populations of harpacticoid copepods (Reidenauer & Thistle 1981),

polychaetes and bivalves (Pridmore et al. 1990). Furthermore, rays have been

implicated in severe damage to commercial shellfish operations (Smith & Merriner

1985; Blaylock 1989; Myers et al. 2007), as well as destroying seagrass beds (Orth

1975; Hovel & Lipcius 2001; Collins et al. 2007).

Despite the abundance and diversity of rays in both tropical and temperate shelf

environments and their effects on benthic assemblages, there have been relatively

few attempts to quantify patterns of bioturbation by these animals. Here, I quantify

bioturbation by rays on soft sediments of a lagoon at Ningaloo Reef in Western

Australia. Given that stingrays move in and out of shallow tidal areas on the reef in

daily cycles (Cerutti-Pereya unpub. data), I hypothesised that new pits would form

after each high tide that allowed access to feeding areas. If rays are highly efficient

feeders, it would be expected that there should be little evidence for re-use of feeding

pits and that pits should infill at relatively constant rates. I tested this hypothesis by

surveying fixed quadrats in a feeding habitat and monitoring rates of infill of pits.

Finally, given that large numbers of rays can inhabit shallow coastal zones, I

examined the amount of sediment turned over by bioturbation by rays in a primary

feeding habitat. In order to give a broader context to the impact of rays on sediments,

I surveyed ray pit formation over a large area of lagoon and reef (1 km2) that

contained a variety of inter-reefal habitats.

Material and Methods

Study Locations

This study was conducted at two locations within the Ningaloo Reef Marine Park,

Western Australia; Mangrove Bay (-21.9762, 113.9598) in the north and Coral Bay

(-23.1335, 113.7703) in the lower section of the marine park (Figure 1). A marine

protected area (sanctuary zone) in which all fishing is prohibited is in place at

Mangrove Bay and extends for approximately 3 km from the shoreline to the outer

reef and runs 4 km from north to south along the shore. Tidal range of Mangrove

Bay during sampling was ≤ 1 m and the maximum water depth where pits were

surveyed was 1.3 m. The sanctuary zone encompasses a small area of mangroves

that are unique in this environment since they are found in very few other places

within the Marine Park. My study site was the intertidal zone immediately adjacent

to mangroves in the southern half of the bay. Within the bay, a large sand spit acts a

tidal barrier forcing flooding tides round its head and then into the southern portion

of the bay. Between the spit and the beach an area of approximately 100,000m2 of

muddy sands are exposed at low tide. The northern half of the intertidal zone of the

bay consists of low-profile limestone reef with abundant macroalgae and very little

sand.

At Coral Bay, I sampled an area of approximately1 km² (1,000,000 m2) immediately

south of the main boat launching facility, extending to the southern sanctuary zone

marker. The lagoon within this area was dominated by expanses of sand bordered on

the seaward side by reef with high coral cover, which sheltered the lagoon from

current and swell. Maximum tidal range at Coral Bay was ≤ 1 m and the maximum

depth of the Coral Bay lagoon sampled was 10 m.

Sampling

At Mangrove Bay, a total of 15 quadrats of 100 m² were monitored for seven days in

each of November 2009, September 2010 and February 2011. Pits were measured

after the first high tide each day in order to estimate rates of formation/infill every 24

hours. Quadrats were haphazardly placed in the area of muddy sediments to the

south of the bay and within each quadrat, pits were identified, marked with a tent peg

and high-visibility ribbon and positions recorded using a GPS. There are many

bioturbating organisms that share this environment, so only pits that could be

attributable to rays were included in the sampling and any depression or excavation

which could not be unambiguously identified as due to a stingray was not included

(Figure 2A).

Figure 1: Ningaloo Reef Marine Park and the two study locations, Mangrove Bay and Coral Bay

The length, breadth and depth of pits was measured daily for a week or until the pits

could no longer be discerned from surrounding sediment in order to test hypotheses

relating to infill of pits and re-use by rays. Measurements were made using a tape

measure and precision of measurements was approximately ± 1cm for each pit. Any

new pits were also marked and measured. All pits were examined for any secondary

use by other fauna, such as crabs or juvenile fish (Figure 2B).

Figure 2: (A) New pit created by feeding ray, and (B) degraded pit with Scylla

serrata occupying excavation

In Coral Bay, the lagoon habitat was surveyed for the presence of rays and pits in

depths between 2 and 9 m. This was done in order to give a broader context to the

impact of rays on sediments across a variety of soft-sediment habitats within the

lagoon. Lagoon habitats were mapped and rays and pits recorded three times over this

area in August 2009, August 2010 and February 2011. Observations were made by

two snorkelers towed at 15 and 25 m behind a boat using manta boards (methods

described by Miller & Müller 1999). Up to 15 – 20 transects spaced between 30 – 60

m apart were required to survey the entire area of 1 km2. The variation in numbers of

A B

transects were related to weather conditions and visibility. When there was lower

visibility, transects were spaced closer than in good conditions, in order to ensure that

observers covered the entire sampling area. The first observer would record the

habitat immediately beneath them every 10 s in one of five categories (sand, coral

reef, biogenic rubble, turf algae and seagrass), while the second would record ray pits

and the presence of rays. The position of pits and rays were recorded using a GPS.

The observer also recorded species identity and approximate size of all rays.

Analytical Procedures

To test the hypothesis regarding quantities of sediments being displaced by rays

during activity, at Mangrove Bay I calculated the volume of empty pits by treating

each (n = 108) as a semi-ellipsoid, using the equation:

(Lr × Br × Dr)/2;

where Lr = length radius, Br = breadth radius and Dr = depth radius. Wet weights of

sediment for these volumes were extrapolated using the mean weight of 10, 1-cm³

samples of wet sediment from the same site. The intensity of disturbance created by

rays feeding over the entire bay was determined by summing total pit area and

dividing by the total sampling area to give a percentage of the total area disturbed. In

order to determine the how long the pits persisted in the sediment at Mangrove Bay

over the course of the seven day sampling period I fitted a generalised linear mixed

model (GLMM) using a binomial distribution and a logit link function where the

response variable was presence/absence of pits and the fixed, explanatory variable

was time (day of the sampling period). I therefore modelled the probability of a pit

being present as a function of time. As individual pits were sampled repeatedly over

time, individual pits were coded as a random effect to account for the temporal

dependence structure between the observations. Pits were sampled over three years,

thus pits were nested in years. Models were fit using the lme4 library in R: a

Language and Environment for Statistical Computing (R development core team

2011) where the random effect was the individual pit nested in year. I used an

information-theoretic approach to test for an effect of time by comparing Akaike’s

information criterion corrected for small samples (AICc) (Burnham & Anderson

2002) and the AICc weight (wAICc) of the slope model (probability of a pit being

present ~ time + year/pit) to the intercept-only (null) model (probability of a pit being

present ~ 1 + year/pit). The intercept-only model (or null model) is a model that does

not contain any β (effects), except for an intercept. In this way I compared two models

that were the same, except that one had the effect of interest (time) and one does not.

The wAICc is a measure of the models relative goodness of fit and varies from 0 (no

support) to 1 (complete support) (Burnham & Anderson 2002).

Changes in the volume of pits over the sampling period were also examined using a

linear mixed-effects approach. This analysis aimed to determine if rays were re-using

a previously excavated pit, which would have created an increase in the volume of the

pit over time, or pit volumes remaining static over time. All pits that were present for

less than three days were removed from the analysis, as I could not fit a line to only

two points. Pit volume was modelled as a function of day with the random effect pit

nested in year and this model was compared to the null model as described above.

Data were log transformed and the models fitted using the R library nlme.

Results

Mangrove Bay

A total of 108 pits were sampled over 21 days, equating to 2.42% of the area sampled

and 0.031% of the entire soft-sediment habitat of the Mangrove Bay intertidal zone

(Figure 3). The sediments excavated by rays during this time equated to 1.08 m³ with

a wet weight of 760.8 kg, and the mean volume of pits from all years was 10,064 cm³

(± 1,487 SE). The numbers of pits varied among the three sampling times, but most

notably in November 2009, when only 19 pits were found, accounting for 17.6% of

the total number of pits found over the three sampling periods. In comparison, counts

of pits in September 2010 and February 2011 accounted for 42% (n = 45) and 40% (n

= 44) of total numbers respectively.

Figure 3: Mangrove Bay southern intertidal zone and position of all sampled pits

Pits ranged in volume from 334 cm³ - 100,577 cm³. Approximately 80% were

relatively small (see Fig. S1 available as Supplementary Material to this paper). The

estimated volume of pits also varied among sampling times, with mean volume in

2009 (21,939 cm3 ± 4,774 SE) almost two and half times greater than in 2010 (8,782

cm3 ± 2,507 SE) and three and half times greater than in 2011 (6,302 cm3 ± 1,115

SE).

Longevity

The probability of a pit being present declined over the seven-day sampling period as

indicated by 100% support for the model that included day as a factor (wAIC = 1)

(Table 1). There was an 80% probability of an average pit being present on day one,

with the probability of presence then rapidly declining to a low of 45% around day 4,

to a low of 15% after seven days (Figure 4).

Table 1. Ranked general linear mixed effects models of the probability of a ray pit

being present explained by day and random effects (pit nested in year),

and the volume of ray pits explained by day and random effects (pit

nested in year) LL, maximum log-liklihood; k, number of estimate model

parameters; AICc, Akaike’s Information Criterion for small samples; Δ

AICc, change in AICc relative to the to ranked model ; WAICc, AICc

weight

Figure 4: GLMM predicted probabilities of pit presence over time. The thick line in

the middle represents the predicted probabilities for all pits and the

lighter lines either side are 95% confidence intervals

Secondary use

There was little evidence for a relationship between volume of the pit and day of

sampling (Figure 2) as the intercept only model (null) had majority support (91%)

(Table 1). Thus, on average, pit volumes remained static over the sampling time,

suggesting that re-use of pits by rays or other species was occurring. As the binomial

model suggested that probability of a pit being present declined over the sampling

period, it would have been reasonable to expect that the model for volume should also

show a declining relationship. This did not occur, probably due to the inconsistent

nature of the relationship between volume and day among years and pits, as can be

seen in the individual plots of pits per year

(Figure 5 and Supp. Figures 3 and 4). Overall, a decline between volume and time

occurred in 48% of pits, with the remaining pits showing a

static (22%) or increasing (30%) volume. In 2009, 35% of pits increased in volume

over 7 d (n = 17) (Figure 5); in 2010, 46% of pits increased in volume, (n = 11)

(Supp. Figure 3) and in 2011, 17% of pits increased in volume

(n = 18) (Supp. Figure 4). Of the 22% of pits that did not change in volume

throughout the period of sampling, 12% occurred in 2009 (Figure 5); 36% in 2010

(Supp. Figure 3) and 27% in 2011 (Supp. Figure 4). These results are evidence for re-

use of the pits either by rays or other organisms.

Figure 5: Linear relationships between day of sampling and volume of each of the

pits sampled from November 2009 that were present for three days or

more

Rays were not directly observed re-using pits; however observations did indicate

secondary use by other taxa in all new pits formed during the study. Small fish were

the most common occupants at low tide (90% of all pits), where pits remained full of

water. Adult fish were occasionally seen in larger pits (> 10,000 cm³, n = 7); however,

over half of these were dead or dying, probably as a result of attacks by sea birds.

Invertebrates such as gastropods (Nerita sp.) were found in 87% of all pits.

Accumulation of detrital material and seaweed was common in every pit examined at

low tide, and this in turn created a potential refuge for organisms such as crabs. The

mud crab Scylla serrata was abundant at Mangrove Bay and 25% of pits had at least

one adult inhabiting it on day 1 when sampling began; while newly formed pits were

occupied by this species in 10% of cases within 24 hours.

Coral Bay

The lagoon at Coral Bay was dominated by sand (48%) and coral reef (36%).

Biogenic rubble (6%) and turf algae (10%) were present in all years; however

seagrass (< 1%) was only documented in February 2011 at the far southern end of the

map boundary. Over the three sampling periods, a total of 20 rays from six species

and 37 ray pits were observed, with the highest number of both rays (n = 9) and pits

(n = 14) recorded in the first sampling session during August 2009. A total of 11 pits

and 6 rays were recorded in August 2010 and 12 pits and 5 rays recorded in February

2011. Of the 37 pits, 92% were recorded in sand and 8% were recorded in sand where

turf algae was also present. Six species of ray were sighted during the sampling:

Urogymnus asperrimus (n = 5), Neotrygon kuhlii (n = 4), Taeniura lymma (n = 1),

Himantura uarnak (n = 3), Pastinachus atrus (n = 6) and Taeniura meyeni

(n = 1). Over half (55%) of all rays were buried in sand and of these, all were found

within 2 m of coral, or some form of structure. T. lymma, N.kuhlii and U. asperrimus

were all found immediately adjacent to reef, buried and inactive. T.meyeni was

observed swimming in mid-water, as were two P. atrus. All H. uarnak and the

remaining P.atrus were found feeding or resting in open sandy habitats.

Discussion

Sediment removal

This study shows that rays can be significant agents of bioturbation in the intertidal

area of a coral reef ecosystem. Ray feeding pits over seven days disturbed an average

of 2.42% of an area of intertidal habitat of 500 m². When extrapolated to a year, this

would result in sediment turnover of 42% of the entire intertidal soft-sediment habitat

(~ 42,000 m²) to a mean depth of 5.6 cm. This estimate is comparable to an earlier

study of bioturbation by rays (Dasyatis americana, D. sabina and Gymnura micrura)

in a temperate estuary in South Carolina, where 30% (6000 m²) of the study area was

covered in ray pits during a July sampling period (Grant 1981). Larger volumes of

sediment were reportedly re-worked by Myliobatis californica and Urolophus halleri

at Bahia La Choya in Mexico (Myrick & Flessa 1996). Their study found that these

two species of ray were overturning sediments at an average rate of 1.01 m³/m2/year,

with > 100 new pits formed every 24 hours. In comparison, rays at Mangrove Bay

overturned sediments at the much lower rate of 0.167m³/m2/year.

Comparable Taxa

It is difficult to compare estimates of bioturbation by rays with those of other large

vertebrates in coral reef systems because very few studies exist. The potential for

bioturbation by animals such as the dugong (Dugong dugon) is well recognised, with

numerous studies of the frequency and effects of feeding scars on benthic habitats and

biological communities (Heinsohn & Birch 1972; Nakaoka et al. 2002; Skilleter et al.

2007). However, there has been no attempt to quantify the volume of material or

turnover rates of sediment moved by these animals. In contrast, bioturbation by

invertebrate taxa, notably callianassid shrimps, has been documented extensively in

coral reef systems (Branch & Pringle 1987; Murphy & Kremer 1992; Tudhope &

Scoffin 1984). These shrimps are deep burrowers and the volume of sediment that

they are capable of processing is immense. Myrick and Flessa (1996) estimated that

these shrimps turned over sediment on a sand flat in Mexico at an average of

0.56 m³ /m² /year; a rate 3.5 times greater than the 0.167 m³ /m² /year I recorded for

rays at Mangrove Bay. Similarly, Riddle (1988) found that the physical effects of

powerful cyclones on soft sediments were quickly erased (within 6 weeks) by the

action of callianassid shrimps in the lagoons on the Great Barrier Reef.

Mangrove Bay vs. Coral Bay

This study examined an intertidal sandflat that was adjacent to an important habitat

for juvenile rays and other elasmobranchs. Acoustic tracking studies have shown that

rays, particularly juveniles and adult females are present in this subtidal habitat year-

round and that this area may function as a nursery for a variety of ray species (Cerutti-

Pereya unpub. data). Thus, the rates of bioturbation I recorded in this area may not be

representative of the wider lagoon of Ningaloo Reef. My surveys of the southern

lagoon suggest that this is the case. Sampling over 1,500 m2 of the sandflat at

Mangrove Bay recorded 108 feeding pits, while manta tows over 1 km2 of the lagoon

at Coral Bay recorded only 37 pits during three surveys. However, it is likely that the

greater current flows and ‘clean’ sand in the lagoon at Coral Bay result in much faster

disintegration of feeding pits at this locality than at Mangrove Bay. A total of six

species of ray were sighted by my surveys at Coral Bay. These species

are common throughout Ningaloo Reef (Stevens et al. 2009) and it is likely that they

are responsible for creating the feeding pits at Mangrove Bay. At high tide these rays

move into the intertidal, presumably to feed although these shallow waters may also

provide a refuge from predation. It is probable that I under-estimated numbers of rays

in the lagoon of Coral Bay, since the smaller species tend to be cryptic, either burying

themselves in sediment (e.g. Neotrygon kuhlii) or hiding under reef outcrops (e.g.

Taeniura lymma).

Longevity

The longevity of ray pits has received little attention, despite the possibility that they

create micro-habitats that may differ from surrounding areas in carbon transport,

nutrient regeneration, sediment stability and decomposition processes (Austen et al.

1999). The formation of ray feeding pits may create bio-geochemical gradients that in

low-energy environments may take many days or weeks to infill, which may account

for some of the unexplained variation in the structure and abundance of benthic

communities on smaller (cm – m) spatial scales (Zajac et al. 2003). As expected, I

found a negative relationship between pit presence and time, as pits were not

permanent structures and were subject to in filling. These model results showed that

there was a reduced probability of an average pit remaining after 4 days (~ 40%) and

at the end of the 7-day sampling period there was on average only a

15% probability of a pit still being present. My analysis of the change in pit volume

over time, however, did not always follow the same negative trend. Over the seven

days of monitoring, only 48% of pits in-filled while the rest remained static or

increased in volume. This latter result is

evidence for reuse of pits by other taxa, some of which are known bioturbators, such

as crabs. The slow disintegration of pits at Mangrove Bay was also probably related to

the protection of the habitat from strong wave action and current flow. Given that they

are common and relatively persistent structures in the soft sediment, it is likely that

pits play an important role in shaping population distributions and structures of

infaunal communities (Zajac et al. 2003). It has been proposed that losses of

bioturbating organisms could impair marine ecosystem function (Thrush & Dayton

2002; Lohrer et al. 2004) and yet despite this, few data are available on pit formation

by rays. Biological effects of ray pits are well documented (e.g. VanBlaricom 1982,

Cross & Curran 2000) and typically demonstrate that infaunal communities are

removed by ray feeding, which is followed by a rapid re-colonisation of pits by

ostracods and amphipods (VanBlaricom 1982). On a microbial level, the creation of

pits can allow oxygen to penetrate deeper into sediments, extending the zone of

nitrification (Gilbert et al. 1995) and even affecting the nitrogen cycle compromising

functions of specific bacterial groups (Kogure & Wada 2005). These responses

highlight the importance of pit formation in the ecology of marine soft sediment

environments and any loss of rays in these habitats may lead to changes in lower

trophic and biogeochemical levels.

In conclusion, this study has quantified the persistence of ray pits, rates of infilling

and sediment turnover rates in an intertidal area of a coral reef ecosystem. In doing so,

I have demonstrated that bioturbation by rays can be a significant functional process

in coastal and nearshore environments and may be critical to physical,

biological and chemical processes at least in some intertidal habitats. Despite 42% of

the soft sediment habitat of Mangrove Bay being re-worked on an annual basis, this

rate of turnover was much lower than recorded by earlier studies of bioturbators,

which have tended to focus on temperate marine ecosystems. Furthermore,

bioturbation may be relatively trivial when considered in the context of sediment

turnover by tidal and wave action (Grant 1981). This implies that ray pit formation

might be most relevant to biological communities on micro (cm) and meso (10s m)

rather than meta (100s m – km) scales (Zajac 2004). Future work will examine the

prey and selectivity of ray feeding at Ningaloo Reef and its effects on infaunal

communities.

Acknowledgements

We thank the Department of Environment and Conservation (WA); field volunteers, M.

O’Shea, A. and D. Stark, A. Turco, T. Hill, S. Ridley, T. Espeland and H. Bowers. This study

was funded by the Australian Institute of Marine Science and all sites within the Marine

Park were accessed according to DEC regulation 4, permit number CEOO2624. We thank

the reviewers for their comments on this manuscript.

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Supplementary Material Fig. S1. Volume frequency of all pits sampled at Mangrove Bay

Fig. S2. The log-transformed volume of all pits sampled from 2009, 2010 and 2011 that were present

for three days or more is plotted on the y-axis, against day of sampling on the x-axis. The

un-transformed values are plotted on the opposite y-axis and the fitted line for the

population of pits obtained by the linear mixed effects model is shown.

Fig. S3.

Linear relat

Septembe

tionships bet

er 2010 that

tween day of

were present

f sampling an

t for three da

nd volume o

ays or more.

f each of the

e pits sampledd from

Fig. S4. Linear relat

February

tionships bet

y 2011 that w

tween day of

were present f

f sampling an

for three day

nd volume o

ys or more.

f each of thee pits sampledd from